Cardiac Autonomic Modulation of Heart Rate Recovery in Children with Spina Bifida

Abstract

We aimed to analyse cardiac autonomic control by assessing the post-exercise heart rate recovery (HRR) and physical fitness in children and adolescents with spina bifida (SB), compared to participants with typical development. A total of 124 participants, 42 with spina bifida (SB group) and 82 typical developmental controls (CO group) performed the arm cranking exercise test with a gas analysis system. HRR was determined at the first (HRR_1) and second (HRR_2) minute at recovery phase. Data are shown as [mean difference (95% CI)]. The SB group showed reduced HR reserve [14.5 (7.1–22.0) bmp, P<0.01], slower HRR_1 [12.4 (7.4–17.5) bpm, P<0.01] and HRR_2 [16.3 (10.6–21.9) bpm; P<0.01], lower VO_2peak [VO_2peak relative: 7.3 (4.2–10.3) mL·min⁻¹·kg⁻¹, P<0.01; VO_2peak absolute: 0.42 (0.30–0.54) L·min⁻¹, P<0.01], and lower O₂ pulse [2.5 (1.8–3.2) mL·bpm, P<0.01] and ventilatory responses [13.5 (8.8–18.1) L·min⁻¹, P<0.01] than the CO group. VE/VO₂ was not different between groups [−2.82 (−5.77– −0.12); P=0.06], but the VE/VCO₂ [−2.59 (−4.40–0.78); P<0.01] and the values of the anaerobic threshold corrected by body mass [−3.2 (−5.8– −0.6) mL·min⁻¹·kg⁻¹, P=0.01] were higher in the SB group than in the CO group. We concluded that children and adolescents with SB have reduced physical fitness and a slower HRR response after maximal effort.

Key words

autonomic nervous system - oxygen uptake - aerobic exercise - upper limbs - wheelchair

Publication History

Article published online:
22 April 2021

• References

• 1 Okutucu S, Karakulak UN, Aytemir K. et al. Heart rate recovery: A practical clinical indicator of abnormal cardiac autonomic function. Expert Rev Cardiovasc Ther 2011; 9: 1417-1430 DOI: 10.1586/erc.11.149.
• 2 Coolbaugh CL, Anderson IB, Wilson MD. et al. Evaluation of an exercise field test using heart rate monitors to assess cardiorespiratory fitness and heart rate recovery in an asymptomatic population. PLoS One 2014; 9: e97704 DOI: 10.1586/erc.11.149.
• 3 La Rovere MT, Pinna GD, Maestri R. et al. Short-term heart rate variability strongly predicts sudden cardiac death in chronic heart failure patients. Circulation 2003; 107: 565-570 DOI: 10.1161/01.cir.0000047275.25795.17.
• 4 Lazic JS, Dekleva M, Soldatovic I. et al. Heart rate recovery in elite athletes: the impact of age and exercise capacity 2017; 117-123
• 5 Figoni SF. Exercise responses and quadriplegia. Med Sci Sports Exerc 1993; 25: 433-441
• 6 Buffart LM, van den Berg-Emons RJG, van Wijlen-Hempel MS. et al. Health-related physical fitness of adolescents and young adults with myelomeningocele. Eur J Appl Physiol 2008; 103: 181-188 DOI: 10.1007/s00421-008-0684-z.
• 7 van den Berg-Emons HJ, Bussmann JB, Brobbel AS. et al. Everyday physical activity in adolescents and young adults with meningomyelocele as measured with a novel activity monitor. J Pediatr 2001; 139: 880-886 DOI: 10.1067/mpd.2001.119991.
• 8 Hansen SE, Hasselstrøm H, Grønfeldt V. et al. Cardiovascular disease risk factors in 6-7-year-old Danish children: the Copenhagen School Child Intervention Study. Prev Med 2005; 40: 740-746 DOI: 10.1016/j.ypmed.2004.09.017.
• 9 Tollerz LUB, Olsson RM, Forslund AH. et al. Reliability of energy cost calculations in children with cerebral palsy, cystic fibrosis and healthy controls. Acta Paediatr 2011; 100: 1616-1620
• 10 Veijalainen A, Haapala EA, Väistö J. et al. Associations of physical activity, sedentary time, and cardiorespiratory fitness with heart rate variability in 6- to 9-year-old children: the PANIC study. Eur J Appl Physiol 2019; 119: 2487-2498 DOI: 10.1007/s00421-019-04231-5.
• 11 Meneghelo R, Araújo C, Stein R. et al. III Diretrizes da Sociedade Brasileira de Cardiologia sobre teste ergométrico. Arq Bras Cardiol 2010; 95: 1-26
• 12 Mesquita ET, Jorge AJL. Entendendo a disfunção diastólica assintomática na prática clínica. Arq Bras Cardiol 2013; 100: 94-101 DOI: 10.1590/S0066-782X2013000100015.
• 13 Cooper DM, Leu S-Y, Galassetti P. et al. Dynamic interactions of gas exchange, body mass, and progressive exercise in children. Med Sci Sports Exerc 2014; 46: 877-886 DOI: 10.1249/MSS.0000000000000180.
• 14 Leonardi-Figueiredo MM, de Souza HCD, Martins EJ. et al. Damaged cardiovascular autonomic control in wheelchair-using children and adolescents with myelomeningocele: a case–control study. Braz J Phys Ther 2019; 23: 27-32 DOI: 10.1016/j.bjpt.2018.09.001.
• 15 Bloemen MAT, van den Berg-Emons RJG, Tuijt M. et al. Physical activity in wheelchair-using youth with spina bifida: An observational study. J Neuroeng Rehabil 2019; 16: 9
• 16 Harriss DJ, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817 DOI: 10.1055/a-1015-3123.
• 17 Rotenstein D, Adams M, Reigel DH. Adult stature and anthropomorphic measurements of patients with myelomeningocele. Eur J Pediatr 1995; 154: 398-402 DOI: 10.1007/BF02072114.
• 18 Dosa NP, Foley JT, Eckrich M. et al. Obesity across the lifespan among persons with spina bifida. Disabil Rehabil 2009; 31: 914-920 DOI: 10.1080/09638280802356476.
• 19 Guedes DP, Guedes JERP. Medida da atividade física em jovens brasileiros: Reprodutibilidade e validade do PAQ-C e do PAQ-A. Rev Bras Med Esporte 2015; 21: 425-432
• 20 Tanner JM. Growth at Adolescence, 2nd Ed. Oxford: Blackwell Scientific Publications. 1962
• 21 Fess EE, Moran CA. Clinical Assessment Recommendations. American Society of Hand Therapists. 1981
• 22 Takken T, Bongers BC, van Brussel M. et al. Cardiopulmonary Exercise Testing in Pediatrics. Ann Am Thorac Soc 2017; 14: S123-S128 DOI: 10.1513/AnnalsATS.201611-912FR.
• 23 Novais L, Silva E, Simões R. et al. Anaerobic Threshold by Mathematical Model in Healthy and Post-Myocardial Infarction Men. Int J Sports Med 2015; 37: 112-118 DOI: 10.1055/s-0035-1555776.
• 24 Van Brussel M, Bongers BC, Hulzebos EHJ. et al. A systematic approach to interpreting the cardiopulmonary exercise test in pediatrics. Pediatr Exerc Sci 2019; 31: 194-203
• 25 Rowland TW. Developmental Exercise Physiology. Human Kinetics Publishers, Champaign, United States: 1996
• 26 Bloemen MAT. Physical Fitness and Physical Behavior in (Wheelchair-using) Youth with Spina Bifida. PhD Dissertation, Utrecht University. 2017
• 27 Ahmadian M, Roshan VD, Hosseinzadeh M. Parasympathetic reactivation in children: influence of two various modes of exercise. Clin Auton Res 2015; 25: 207-212 DOI: 10.1007/s10286-015-0289-7.
• 28 Iwasaki KI, Zhang R, Zuckerman JH. et al. Effect of head-down-tilt bed rest and hypovolemia on dynamic regulation of heart rate and blood pressure. Am J Physiol Regul Integr Comp Physiol 2000; 279: R2189-R2199 DOI: 10.1152/ajpregu.2000.279.6.R2189.
• 29 Buker DB, Oyarce CC, Plaza RS. Effects of spinal cord injury in heart rate variability after acute and chronic exercise: A systematic review. Top Spinal Cord Inj Rehabil 2018; 24: 167-176 DOI: 10.1310/sci17-00028.
• 30 García-Hermoso A, Ramírez-Campillo R, Izquierdo M. Is muscular fitness associated with future health benefits in children and adolescents? A systematic review and meta-analysis of longitudinal studies. Sports Med 2019; 49: 1079-1094 DOI: 10.1007/s40279-019-01098-6.
• 31 Souza W, Plavnik F. et al. Hipertensão na criança e no adolescente. Arq Bras Cardiol 2016; 107: 53-63 DOI: 10.5935/abc.20160160.
• 32 Peçanha T, Silva-Júnior ND, Forjaz CL. et al. Heart rate recovery: autonomic determinants, methods of assessment and association with mortality and cardiovascular diseases. Clin Physiol Funct Imaging 2014; 34: 327-339 DOI: 10.1111/cpf.12102.
• 33 Cole CR, Blackstone EH, Pashkow FJ. et al. Heart-rate recovery immediately after exercise as a predictor of mortality. N Engl J Med 1999; 341: 1351-1357 DOI: 10.1056/NEJM199910283411804.
• 34 Qiu S, Cai X, Sun Z. et al. Heart rate recovery and risk of cardiovascular events and all-cause mortality: a meta-analysis of prospective cohort studies. J Am Heart Assoc 2017; 6: e005505 DOI: 10.1161/JAHA.117.005505.
• 35 Morise AP. Heart rate recovery: predictor of risk today and target of therapy tomorrow?. Circulation 2004; 110: 2778-2780 DOI: 10.1161/01.CIR.0000147615.62634.48.
• 36 Ohuchi H, Suzuki H, Yasuda K. et al. Heart rate recovery after exercise and cardiac autonomic nervous activity in children. Pediatr Res 2000; 47: 329-335 DOI: 10.1203/00006450-200003000-00008.
• 37 Singh TP, Rhodes J, Gauvreau K. Determinants of heart rate recovery following exercise in children. Med Sci Sports Exerc 2008; 40: 601-605 DOI: 10.1249/MSS.0b013e3181621ec4.
• 38 Serra-Añó P, Montesinos LL, Morales J. et al. Heart rate variability in individuals with thoracic spinal cord injury. Spinal Cord 2015; 53: 59-63 DOI: 10.1038/sc.2014.207.
• 39 Fu Q, Levine BD. Exercise and the autonomic nervous system. In: Buijs RM, Swaab DF, Eds. Handbook of Clinical Neurology. Elsevier 2013; 147-160 DOI: 10.1016/B978-0-444-53491-0.00013-4.
• 40 Sampaio I, Palma H, Nascimento R. et al. Atividade esportiva na reabilitação. In: Greve J, Casalis M, Barros T. Diagnóstico e Tratamento da Lesão da Medula Espinal. São Paulo: Rocas; 2001
• 41 Tuijtelaars JAM, Leonardi-Figuiredo MM, Crescencio J. et al. Cardiopulmonary exercise test using arm ergometry in children with spina bifida. Pediatr Phys Ther 2019; 31: 185-190 DOI: 10.1097/PEP.0000000000000590.
• 42 De Backer IC, Singh-Grewal D, Helders PJM. et al. Can peak work rate predict peak oxygen uptake in children with juvenile idiopathic arthritis?. Arthritis Care Res (Hoboken) 2010; 62: 960-964 DOI: 10.1002/acr.20153.
• 43 Lin K-H, Lai J-S, Kao M-J. et al. Anaerobic threshold and maximal oxygen consumption during arm cranking exercise in paraplegia. Arch Phys Med Rehabil 1993; 74: 515-520
• 44 Arena R, Myers J, Hsu L. et al. The minute ventilation/carbon dioxide production slope is prognostically superior to the oxygen uptake efficiency slope. J Card Fail 2007; 13: 462-469 DOI: 10.1016/j.cardfail.2007.03.004.
• 45 Patel J, Walker JL, Talwalkar VR. et al. Correlation of spine deformity, lung function, and seat pressure in spina bifida. Clin Orthop Relat Res 2011; 469: 1302-1307 DOI: 10.1007/s11999-010-1687-8.
• 46 de Groot JF, Takken T, de Graaff S. et al. Treadmill testing of children who have spina bifida and are ambulatory: does peak oxygen uptake reflect maximum oxygen uptake?. Phys Ther 2009; 89: 679-687 DOI: 10.2522/ptj.20080328.
• 47 Martins EJ, Gastaldi AC, Davoli GBQ. et al. Decreased respiratory performance of children and adolescents with myelomeningocele who use a wheelchair – preliminary data. Braz J Med Biol Res 2019; 52: e8671 DOI: 10.1590/1414-431x20198671.
• 48 Schneider DA, Sedlock DA, Gass E. et al. V˙O2peak and the gas-exchange anaerobic threshold during incremental arm cranking in able-bodied and paraplegic men. Eur J Appl Physiol Occup Physiol 1999; 80: 292-297 DOI: 10.1007/s004210050595.
• 49 Holloszy JO. Adaptation of skeletal muscle to endurance exercise. Med Sci Sports 1975; 7: 155-164
• 50 Costill DL, Coyle E, Dalsky G. et al. Effects of elevated plasma FFA and insulin on muscle glycogen usage during exercise. J Appl Physiol Respir Environ Exerc Physiol 1977; 43: 695-699 DOI: 10.1152/jappl.1977.43.4.695.
• 51 Turley KR. Cardiovascular responses to exercise in children. Sports Med 1997; 24: 241-257 DOI: 10.2165/00007256-199724040-00003.
• 52 Rutenfranz J, Andersen KL, Seliger V. et al. Maximal aerobic power affected by maturation and body growth during childhood and adolescence. Eur J Pediatr 1982; 139: 106-112 DOI: 10.1007/BF00441491.
• 53 Rowland T, Goff D, Martel L. et al. Influence of cardiac functional capacity on gender differences in maximal oxygen uptake in children. Chest 2000; 117: 629-635 DOI: 10.1378/chest.117.3.629.
• 54 Vinet A, Mandigout S, Nottin S. et al. Influence of body composition, hemoglobin concentration, and cardiac size and function of gender differences in maximal oxygen uptake in prepubertal children. Chest 2003; 124: 1494-1499 Im Internet: https://linkinghub.elsevier.com/retrieve/pii/S0012369216486988
• 55 Winsley RJ, Fulford J, Roberts AC. et al. Sex difference in peak oxygen uptake in prepubertal children. J Sci Med Sport 2009; 12: 647-651 DOI: 10.1378/chest.124.4.1494.
• 56 Mc Narry MA, Farr C, Middlebrooke A. et al. Aerobic Function and muscle deoxygenation dynamics during ramp exercise in children. Med Sci Sports Exerc 2015; 47: 1877-1884 DOI: 10.1249/MSS.0000000000000609.
• 57 Castilho SD, Barras Filho AA. Crescimento pós-menarca. Arq Bras Endocrinol Metab 2000; 44: 195-204 DOI: 10.1590/S0004-27302000000300003.
• 58 Armstrong N, Welsman J. Sex-specific longitudinal modeling of youth peak oxygen uptake. Pediatr Exerc Sci 2019; 31: 204-212 DOI: 10.1123/pes.2018-0175.
• 59 Engin A. The definition and prevalence of obesity and metabolic syndrome. 2017; 1-17 DOI: 10.1007/978-3-319-48382-5_1.
• 60 Jouven X, Empana J-P, Schwartz PJ. et al. Heart-rate profile during exercise as a predictor of sudden death. N Engl J Med 2005; 352: 1951-1958